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Abnormal Locus Coeruleus Sleep Activity Alters Sleep Signatures of Memory Consolidation and Impairs Place Cell Stability and Spatial Memory
Open accessAbstract
Sleep is critical for proper memory consolidation. The locus coeruleus (LC) releases norepinephrine throughout the brain except when the LC falls silent throughout rapid eye movement (REM) sleep and prior to each non-REM (NREM) sleep spindle. We hypothesize that these transient LC silences allow the synaptic plasticity that is necessary to incorporate new information into pre-existing memory circuits. We found that spontaneous LC activity within sleep spindles triggers a decrease in spindle power. By optogenetically stimulating norepinephrine-containing LC neurons at 2 Hz during sleep, we reduced sleep spindle occurrence, as well as NREM delta power and REM theta power, without causing arousals or changing sleep amounts. Stimulating the LC during sleep following a hippocampus-dependent food location learning task interfered with consolidation of newly learned locations and reconsolidation of previous locations, disrupting next-day place cell activity. The LC stimulation-induced reduction in NREM sleep spindles, delta, and REM theta and reduced ripple-spindle coupling all correlated with decreased hippocampus-dependent performance on the task. Thus, periods of LC silence during sleep following learning are essential for normal spindle generation, delta and theta power, and consolidation of spatial memories.
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Cites
Normality Tests for Statistical Analysis: A Guide for Non-Statisticians
Ghasemi, A., & Zahediasl, S. (2012) · International Journal of Endocrinology and Metabolism · doi:10.5812/ijem.3505 · Cited by 4,368 · cited 1×
“All data sets were first tested for normality using Shapiro-Wilk normality test as recommended [55].”
Thalamocortical oscillations in the sleeping and aroused brain
Steriade, M., McCormick, D. A., & Sejnowski, T. J. (1993) · Science · doi:10.1126/science.8235588 · Cited by 3,564
Berridge, C. W., & Waterhouse, B. D. (2003) · Brain Research Reviews · doi:10.1016/s0165-0173(03)00143-7 · Cited by 2,529
Aston-Jones, G., & Bloom, F. (1981) · The Journal of Neuroscience · doi:10.1523/jneurosci.01-08-00876.1981 · Cited by 1,960
Self-citationThe locus coeruleus and noradrenergic modulation of cognition
Sara, S. J. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2573 · Cited by 1,848
Self-citationBoosting slow oscillations during sleep potentiates memory
Marshall, L., Helgadóttir, H., Mölle, M., & Born, J. (2006) · Nature · doi:10.1038/nature05278 · Cited by 1,792
Coordinated memory replay in the visual cortex and hippocampus during sleep
Ji, D., & Wilson, M. A. (2007) · Nature Neuroscience · doi:10.1038/nn1825 · Cited by 1,669
Selective suppression of hippocampal ripples impairs spatial memory
Girardeau, G., Benchenane, K., Wiener, S. I., Buzsáki, G., & Zugaro, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn.2384 · Cited by 1,560
β-Adrenergic activation and memory for emotional events
Cahill, L., Prins, B., Weber, M., & McGaugh, J. L. (1994) · Nature · doi:10.1038/371702a0 · Cited by 1,271
Coordinated interactions between hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep
Siapas, A. G., & Wilson, M. A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80629-7 · Cited by 1,052
Tuning arousal with optogenetic modulation of locus coeruleus neurons
Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., Deisseroth, K., & de Lecea, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2682 · Cited by 993
Communication between neocortex and hippocampus during sleep in rodents
Sirota, A., Csicsvari, J., Buhl, D., & Buzsáki, G. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437938100 · Cited by 930
Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation
Boyce, R., Glasgow, S. D., Williams, S., & Adamantidis, A. (2016) · Science · doi:10.1126/science.aad5252 · Cited by 696
Hippocampo-cortical coupling mediates memory consolidation during sleep
Maingret, N., Girardeau, G., Todorova, R., Goutierre, M., & Zugaro, M. (2016) · Nature Neuroscience · doi:10.1038/nn.4304 · Cited by 667
Kempadoo, K. A., Mosharov, E. V., Choi, S. J., Sulzer, D., & Kandel, E. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1616515114 · Cited by 647
Sleep, Plasticity and Memory from Molecules to Whole-Brain Networks
Abel, T. G., Havekes, R., Saletin, J., & Walker, M. P. (2013) · Current Biology · doi:10.1016/j.cub.2013.07.025 · Cited by 585
Visual Discrimination Task Improvement: A Multi-Step Process Occurring During Sleep
Stickgold, R., Whidbee, D., Schirmer, B., Patel, V., & Hobson, J. A. (2000) · Journal of Cognitive Neuroscience · doi:10.1162/089892900562075 · Cited by 560
REM sleep selectively prunes and maintains new synapses in development and learning
Li, W., Ma, L., Yang, G., & Gan, W.-B. (2017) · Nature Neuroscience · doi:10.1038/nn.4479 · Cited by 543
Experience-dependent, asymmetric expansion of hippocampal place fields
Mehta, M. R., Barnes, C. A., & McNaughton, B. L. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.16.8918 · Cited by 536
Daytime naps, motor memory consolidation and regionally specific sleep spindles
Nishida, M., & Walker, M. P. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000341 · Cited by 531
Homer1a drives homeostatic scaling-down of excitatory synapses during sleep
Diering, G. H., Nirujogi, R. S., Roth, R. H., Worley, P. F., Pandey, A., & Huganir, R. L. (2017) · Science · doi:10.1126/science.aai8355 · Cited by 516
An Information-Theoretic Approach to Deciphering the Hippocampal Code
Skaggs, W. E., McNaughton, B. L., & Gothard, K. M. (1992) · Cited by 511
Experience-Dependent Asymmetric Shape of Hippocampal Receptive Fields
Mehta, M. R., Quirk, M. C., & Wilson, M. A. (2000) · Neuron · doi:10.1016/s0896-6273(00)81072-7 · Cited by 488
Sleep spindle activity is associated with the integration of new memories and existing knowledge
Tamminen, J., Payne, J. D., Stickgold, R., Wamsley, E. J., & Gaskell, M. G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.3028-10.2010 · Cited by 478
Przybyslawski, J., Roullet, P., & Sara, S. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06623.1999 · Cited by 470
Self-citationThompson, L. T., & Best, P. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90555-p · Cited by 386
Novelty acquisition is associated with induction of hippocampal long-term depression
Manahan‐Vaughan, D., & Braunewell, K. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.15.8739 · Cited by 358
The Critical Role of Sleep Spindles in Hippocampal-Dependent Memory: A Pharmacology Study
Mednick, S. C., McDevitt, E. A., Walsh, J. K., Wamsley, E. J., Paulus, M. P., Kanady, J. C., & Drummond, S. P. A. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3127-12.2013 · Cited by 336
Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep
Poe, G. R., Nitz, D. A., McNaughton, B. L., & Barnes, C. A. (2000) · Brain Research · doi:10.1016/s0006-8993(99)02310-0 · Cited by 318
Self-citationRoozendaal, B., Nguyen, B. T., Power, A. E., & McGaugh, J. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.20.11642 · Cited by 293
State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep
Wierzynski, C. M., Lubenov, E. V., Gu, M., & Siapas, A. G. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.011 · Cited by 289
Locus coeruleus input to hippocampal CA3 drives single-trial learning of a novel context
Wagatsuma, A., Okuyama, T., Sun, C., Smith, L. M., Abe, K., & Tonegawa, S. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714082115 · Cited by 283
Elevated Sleep Spindle Density after Learning or after Retrieval in Rats
Eschenko, O., Mölle, M., Jan Born, A., & Sara, S. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3175-06.2006 · Cited by 268
Self-citationNMDA Receptor Antagonism Blocks Experience-Dependent Expansion of Hippocampal “Place Fields”
Ekstrom, A. D., Meltzer, J., McNaughton, B. L., & Barnes, C. A. (2001) · Neuron · doi:10.1016/s0896-6273(01)00401-9 · Cited by 246
Noradrenergic Regulation of Synaptic Plasticity in the Hippocampal CA1 Region
Katsuki, H., Izumi, Y., & Zorumski, C. F. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3013 · Cited by 244
Sharp wave ripples during learning stabilize the hippocampal spatial map
Roux, L., Hu, B., Eichler, R., Stark, E., & Buzsáki, G. (2017) · Nature Neuroscience · doi:10.1038/nn.4543 · Cited by 229
Sara, S. J., & Segal, M. (1991) · Progress in brain research · doi:10.1016/s0079-6123(08)63835-2 · Cited by 223
Self-citationLearning increases human electroencephalographic coherence during subsequent slow sleep oscillations
Mölle, M., Marshall, L., Gais, S., & Born, J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402820101 · Cited by 222
Nocturnal/daytime urine noradrenergic measures and sleep in combat-related PTSD
Mellman, T. A., Kumar, A., Kulick-Bell, R., Kumar, M., & Nolan, B. (1995) · Biological Psychiatry · doi:10.1016/0006-3223(94)00238-x · Cited by 219
Eschenko, O., Magri, C., Panzeri, S., & Sara, S. J. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr121 · Cited by 194
Self-citationThe Role of Slow Wave Sleep in Memory Processing.
Walker, M. P. (2009) · Journal of Clinical Sleep Medicine · doi:10.5664/jcsm.5.2s.s20 · Cited by 177
O'Dell, T. J., Connor, S. A., Guglietta, R., & Nguyen, P. V. (2015) · Learning & Memory · doi:10.1101/lm.031088.113 · Cited by 163
Long-Term Depression: A Cellular Basis for Learning?
Braunewell, K., & Manahan‐Vaughan, D. (2001) · Reviews in the Neurosciences · doi:10.1515/revneuro.2001.12.2.121 · Cited by 160
Kaestner, E. J., Wixted, J. T., & Mednick, S. C. (2013) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00433 · Cited by 149
Deep sleep maintains learning efficiency of the human brain
Fattinger, S., de Beukelaar, T. T., Ruddy, K. L., Volk, C., Heyse, N. C., Herbst, J. A., Hahnloser, R. H. R., Wenderoth, N., & Huber, R. (2017) · Nature Communications · doi:10.1038/ncomms15405 · Cited by 148
Poe, G. R. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0820-16.2017 · Cited by 142
Self-citationGazarini, L., Stern, C. A. J., Carobrez, A. P., & Bertoglio, L. J. (2013) · Learning & Memory · doi:10.1101/lm.030007.112 · Cited by 122
Novitskaya, Y., Sara, S. J., Logothetis, N. K., & Eschenko, O. (2016) · Learning & Memory · doi:10.1101/lm.040923.115 · Cited by 116
Self-citationEschenko, O., & Sara, S. J. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn020 · Cited by 115
Self-citationBrain aminergic axons exhibit marked variability in conduction velocity
Aston‐Jones, G., Segal, M., & Bloom, F. E. (1980) · Brain Research · doi:10.1016/0006-8993(80)90880-x · Cited by 110
Self-citationDetection of seven sleep-waking stages in the rat
Gottesmann, C. (1992) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(05)80048-x · Cited by 110
Sara, S. J. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0297-16.2017 · Cited by 107
Self-citationLi, Y., Hickey, L., Perrins, R., Werlen, E., Patel, A. A., Hirschberg, S., Jones, M. W., Salinas, S., Kremer, E. J., & Pickering, A. E. (2016) · Brain Research · doi:10.1016/j.brainres.2016.02.023 · Cited by 97
Self-citationLee, K. H., & McCormick, D. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80162-2 · Cited by 85
Aston‐Jones, G., Foote, S. L., & Segal, M. (1985) · Neuroscience · doi:10.1016/0306-4522(85)90077-6 · Cited by 77
Self-citationWatts, A., Gritton, H. J., Sweigart, J., & Poe, G. R. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0170-12.2012 · Cited by 75
Self-citationREM restriction persistently alters strategy used to solve a spatial taskPreprint
Bjorness, T. E., Riley, B. T., Tysor, M. K., & Poe, G. R. (2005) · Learning & Memory · doi:10.1101/lm.84805 · Cited by 70
Self-citationGross, B. A., Walsh, C. M., Turakhia, A. A., Booth, V., Mashour, G. A., & Poe, G. R. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.07.009 · Cited by 58
Self-citationFuhs, M. C., VanRhoads, S. R., Casale, A. E., McNaughton, B., & Touretzky, D. S. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00132.2005 · Cited by 53
Different simultaneous sleep states in the hippocampus and neocortex
Emrick, J. J., Gross, B. A., Riley, B. T., & Poe, G. R. (2016) · Sleep · doi:10.5665/sleep.6326 · Cited by 38
Self-citationBooth, V., & Poe, G. R. (2006) · Hippocampus · doi:10.1002/hipo.20143 · Cited by 36
Self-citationA spatial memory task appropriate for electrophysiological recordings
Poe, G. R., Thompson, C. M., Riley, B. T., Tysor, M. K., Bjorness, T. E., Steinhoff, B. P., & Ferluga, E. D. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00233-9 · Cited by 10
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Metadata
- Authors
- Swift, K. M., Gross, B. A., Frazer, M. A., Bauer, D. S., Clark, K. J. D., Vazey, E. M., Aston-Jones, G., Li, Y., Pickering, A. E., Sara, S. J., & Poe, G. R.
- Affiliations
- University of Michigan (US)
- University of California, Los Angeles (US)
- University of Massachusetts Amherst (US)
- University of Bristol (GB)
- Collège de France (FR)
- Corresponding author
- Poe, Gina R.
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2018-11
- Volume
- 28
- Issue
- 22
- Pages
- 3599-3609.e4
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC7556718
- OpenAlex
- W2899315813
- Cited by
- 158
- References
- 62
- Citations by year
- 2026: 19 · 2025: 34 · 2024: 21 · 2023: 25 · 2022: 19 · 2021: 19 · 2020: 12 · 2019: 8 · 2018: 1
- FWCI
- 5.95
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 383 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Bristol Research (University of Bristol) (acceptedVersion, cc-by-nc-nd)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Explore Bristol Research (submittedVersion, cc-by-nc-nd)
- Funders
- NIMH (R01 60670, br088373)
- Wellcome Senior Clinical
- University of Michigan Systems and Integrative Biology T32
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- locus coeruleus, norepinephrine, sleep spindles, memory consolidation, spatial memory, REM sleep, NREM sleep, hippocampus-dependent learning, memory reconsolidation, optogenetic stimulation, synaptic plasticity
- MeSH terms
- Memory Consolidation, Place Cells, Sleep, Slow-Wave, Animals, Brain, Electroencephalography, Hippocampus, Locus Coeruleus, Male, Sleep, Sleep Stages, Sleep, REM, Theta Rhythm, Rats, Long-Evans, Rats, CA1 Region, Hippocampal, Spatial Memory
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